Muscleblind proteins regulate alternative splicing

EMBO Journal

Volumn 23, Issue 15, 2004, Pages 3103-3112

  Ho, Thai H ^a   Charlet B, Nicolas ^a,c   Poulos, Michael G ^b   Singh, Gopal ^a   Swanson, Maurice S ^b   Cooper, Thomas A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

Alternative splicing; CELF proteins; CUG BP1; Muscleblind; Myotonic dystrophy

Indexed keywords

CELF PROTEIN; INSULIN RECEPTOR; MESSENGER RNA PRECURSOR; MUSCLEBLIND PROTEIN; PROTEIN; SMALL INTERFERING RNA; TROPONIN T; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; ARTICLE; BINDING SITE; CONTROLLED STUDY; EXON; HUMAN; HUMAN CELL; INTRON; MYOTONIC DYSTROPHY; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY MECHANISM;

ALTERNATIVE SPLICING; ANIMALS; BASE SEQUENCE; BINDING SITES; CELL LINE; CHICKENS; EXONS; HUMANS; INTRONS; RATS; RECEPTOR, INSULIN; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS; TROPONIN T;

EID: 4143120231     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600300     Document Type: Article

References (54)

1. Artero R, Prokop A, Paricio N, Begemann G, Pueyo I, Mlodzik M, Perez-Alonso M, Baylies MK (1998) The muscleblind gene participates in the organization of Z-bands and epidermal attachments of Drosophila muscles and is regulated by Dmef2. Dev Biol 195: 131-143
2. Ashiya M, Grabowski PJ (1997) A neuron-specific splicing switch mediated by an array of pre-mRNA repressor sites: evidence of a regulatory role for the polypyrimidine tract binding protein and a brain-specific PTB counterpart. RNA 3: 996-1015
3. Bai C, To lias PP (1996) Cleavage of RNA hairpins mediated by a developmentally regulated CCCH zinc finger protein. Mol Cell Biol 16: 6661-6667
4. Bai C, Tolias PP (1998) Drosophila clipper/CPSF 30 K is a post-transcriptionally regulated nuclear protein that binds RNA containing GC clusters. Nucleic Acids Res 26: 1597-1604
5. Begemann G, Paricio N, Artero R, Kiss I, Perez-Alonso M, Mlodzik M (1997) Muscleblind, a gene required for photoreceptor differentiation in Drosophila, encodes novel nuclear Cys3His-type zinc-finger-containing proteins. Development 124: 4321-4331
6. Black DL (2003) Mechanisms of alternative Pre-messenger RNA splicing. Annu Rev Biochem 27: 27-48
7. Brook JD, McCurrach ME, Harley HG, Buckler AJ, Church D, Aburatani H, Hunter K, Stanton VP, Thirion JP, Sohn R, Zemelman B, R.G S, Rundle SA, Crow S, Davies J, Shelbourne P, Buxton J, Jones C, Juvonen V, Johnson K, Harper PS, Shaw DJ, Housman DE, (1992) Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member. Cell 68: 799-808
8. Buj-Bello A, Furling D, Tronchere H, Laporte J, Lerouge T, Butler-Browne GS, Mandel JL (2002) Muscle-specific alternative splicing of myotubularin-related 1 gene is impaired in DM1 muscle cells. Hum Mol Genet 11: 2297-2307
9. Chan RC, Black DL (1997) The polypyrimidine tract binding protein binds upstream of neural cell-specific c-src exon N1 to repress the splicing of the intron downstream. Mol Cell Biol 17: 4667-4676
10. Charlet-B N, Logan P, Singh G, Cooper TA (2002a) Dynamic antagonism between ETR-3 and PTB regulates cell type-specific alternative splicing. Mol Cell 9: 649-658
11. Charlet-B N, Savkur RS, Singh G, Philips AV, Grice EA, Cooper TA (2002b) Loss of the muscle-specific chloride channel in type 1 myotonic dystrophy due to misregulated alternative splicing. Mol Cell 10: 45-53
12. Cheng Y, Kato N, Wang W, Li J, Chen X (2003) Two RNA binding proteins, HEN4 and HUA1, act in the processing of AGAMOUS pre-mRNA in Arabidopsis thaliana. Dev Cell 4: 53-66
13. Cooper TA (1998) Muscle-specific splicing of a heterologous exon mediated by a single muscle-specific splicing enhancer from the cardiac troponin T gene. Mol Cell Biol 18: 4519-4525
14. Davis BM, McCurrach ME, Taneja KL, Singer RH, Housman DE (1997) Expansion of a CUG trinucleotide repeat in the 3′ untranslated region of myotonic dystrophy protein kinase transcripts results in nuclear retention of transcripts. Proc Natl Acad Sci USA 94: 7388-7393
15. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498
16. Fardaei M, Larkin K, Brook JD, Hamshere MG (2001) In vivo colocalisation of MBNL protein with DMPK expanded-repeat transcripts. Nucleic Acids Res 29: 2766-2771
17. Fardaei M, Rogers MT, Thorpe HM, Larkin K, Hamshere MG, Harper PS, Brook JD (2002) Three proteins, MBNL, MBLL and MBXL, colocalize in vivo with nuclear foci of expanded-repeat transcripts in DM1 and DM2 cells. Hum Mol Genet 11: 805-814
18. Faustino NA, Cooper TA (2003) Pre-mRNA splicing and human disease. Genes Dev 17: 419-437
19. Fu YH, Pizzuti A, Fenwick RG, King J, Rajnarayan S, Dunne PW, Dubel J, Nasser GA, Ashizawa T, Dejong P, Wieringa B, Korneluk R, Ferryman MB, Epstein HF, Caskey CT (1992) An unstable triplet repeat in a gene related to myotonic muscular dystrophy. Science 255: 1256-1258
20. Good PJ, Chen Q, Warner SJ, Herring DC (2000) A family of human RNA-binding proteins related to the Drosophila Bruno translational regulator. J Biol Chem 275: 28583-28592
21. Herbert A (2004) The four Rs of RNA-directed evolution. Nat Genet 36: 19-25
22. Jin W, McCutcheon IE, Fuller GN, Huang ES, Cote GJ (2000) Fibroblast growth factor receptor-1 alpha-exon exclusion and polypyrimidine tract-binding protein in glioblastoma multiforme tumors. Cancer Res 60: 1221-1224
23. Kanadia RN, Johnstone KA, Mankodi A, Lungu C, Thornton CA, Esson D, Timmers AM, Hauswirth WW, Swanson MS (2003) A muscleblind knockout model for myotonic dystrophy. Science 302: 1978-1980
24. Kino Y, Mori D, Oma Y, Takeshita Y, Sasagawa N, Ishiura S (2004) Muscleblind protein, MBNL1/EXP, binds specifically to CHHG repeats. Hum Mol Genet 13: 495-507
25. Kosaki A, Nelson J, Webster NJ (1998) Identification of intron and exon sequences involved in alternative splicing of insulin receptor pre-mRNA. J Biol Chem 273: 10331-10337
26. Ladd AN, Charlet-B N, Cooper TA (2001) The CELF family of RNA binding proteins is implicated in cell-specific and developmental regulated alternative splicing. Mol Cell Biol 21: 1285-1296
27. Ladd AN, Nguyen NH, Malhotra K, Cooper TA (2004) CELF6, a member of the CELF family of RNA binding proteins, regulates MSB-dependent alternative splicing. J Biol Chem 279: 17756-17764
28. Lai WS, Carballo E, Strum JR, Kennington EA, Phillips RS, Blackshear PJ (1999) Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 19: 4311-4323
29. Liquori CL, Ricker K, Moseley ML, Jacobsen JF, Kress W, Naylor SL, Day JW, Ranum LP (2001) Myotonic dystrophy type 2 caused by a CCTG expansion in intron 1 of ZNF9. Science 293: 864-867
30. Mahadevan M, Tsilfidis C, Sabourin L, Shutler G, Amemiya C, Jansen G, Neville C, Narang M, Barcelo J, Ohoy K, Leblond S, Earlemacdonald J, Dejong PJ, Wieringa B, Korneluk RG (1992) Myotonic dystrophy mutation-an unstable CTG repeat in the 3′ untranslated region of the gene. Science 255: 1253-1255
31. Mankodi A, Logigian E, Callahan L, McClain C, White R, Henderson D, Krym M, Thornton CA (2000) Myotonic dystrophy in transgenic mice expressing an expanded CUG repeat. Science 289: 1769-1773
32. Mankodi A, Takahashi MP, Jiang H, Beck CL, Bowers WJ, Moxley RT, Cannon SC, Thornton CA (2002) Expanded CUG repeats trigger aberrant splicing of ClC-1 chloride channel pre-mRNA and hyperexcitability of skeletal muscle in myotonic dystrophy. Mol Cell 10: 35-44
33. Mankodi A, Urbinati CR, Yuan QP, Moxley RT, Sansone V, Krym M, Henderson D, Schalling M, Swanson MS, Thornton CA (2001) Muscleblind localizes to nuclear foci of aberrant RNA in myotonic dystrophy types 1 and 2. Hum Mol Genet 10: 2165-2170
34. Michalowski S, Miller JW, Urbinati CR, Paliouras M, Swanson MS, Griffith J (1999) Visualization of double-stranded RNAs from the myotonic dystrophy protein kinase gene and interactions with CUG-binding protein. Nucleic Acids Res 27: 3534-3542
35. Michel SL, Guerrerio AL, Berg JM (2003) Selective RNA binding by a single CCCH zinc-binding domain from Nup475 (Tristetraprolin). Biochemistry 42: 4626-4630
36. Miller JW, Urbinati CR, Teng-Umnuay P, Stenberg MG, Byrne BJ, Thornton CA, Swanson MS (2000) Recruitment of human muscleblind proteins to (CUG)n expansions associated with myotonic dystrophy. EMBO J 19: 4439-4448
37. Mukhopadhyay D, Houchen CW, Kennedy S, Dieckgraefe BK, Anant S (2003) Coupled mRNA stabilization and translational silencing of cyclooxygenase-2 by a novel RNA binding protein, CUGBP2. Mol Cell 11: 113-126
38. Philips AV, Timchenko LT, Cooper TA (1998) Disruption of splicing regulated by a CUG-binding protein in myotonic dystrophy. Science 280: 737-741
39. Polydorides AD, Okano HJ, Yang YY, Stefani G, Darnell RB (2000) A brain-enriched polypyrimidine tract-binding protein antagonizes the ability of Nova to regulate neuron-specific alternative splicing. Proc Natl Acad Sci USA 97: 6350-6355
40. Ryan KJ, Cooper TA (1996) Muscle-specific splicing enhancers regulate inclusion of the cardiac troponin T alternative exon in embryonic skeletal muscle. Mol Cell Biol 16: 4014-4023
41. Savkur RS, Philips AV, Cooper TA (2001) Aberrant regulation of insulin receptor alternative splicing is associated with insulin resistance in myotonic dystrophy. Nat Genet 29: 40-47
42. Savkur RS, Philips AV, Cooper TA, Dalton JC, Moseley ML, Ranum LP, Day JW (2004) Insulin receptor splicing alteration in myotonic dystrophy type 2. Am J Hum Genet 74: 1309-1313
43. Sergeant N, Sablonniere B, Schraen-Maschke S, Ghestem A, Maurage CA, Wattez A, Vermersch P, Delacourte A (2001) Dysregulation of human brain microtubule-associated tau mRNA maturation in myotonic dystrophy type 1. Hum Mol Genet 10: 2143-2155
44. Singh G, Charlet BN, Han J, Cooper TA (2004) ETR-3 and CELF4 protein domains required for RNA binding and splicing activity in vivo. Nucleic Acids Res 32: 1232-1241
45. Sobczak K, de Mezer M, Michlewski G, Krol J, Krzyzosiak WJ (2003) RNA structure of trinucleotide repeats associated with human neurological diseases. Nucleic Acids Res 31: 5469-5482
46. Squillace RM, Chenault DM, Wang EH (2002) Inhibition of muscle differentiation by the novel muscleblind-related protein CHCR. Dev Biol 250: 218-230
47. Stamm S, Casper D, Hanson V, Helfman DM (1999) Regulation of the neuron-specific exon of clathrin light chain B. Brain Res Mol Brain Res 64: 108-118
48. Stoecklin G, Colombi M, Raineri I, Leuenberger S, Mallaun M, Schraidlin M, Gross B, Lu M, Kitamura T, Moroni C (2002) Functional cloning of BRF1, a regulator of ARE-dependent mRNA turnover. EMBO J 21: 4709-4718
49. Taneja KL, McCurrach M, Schalling M, Housman D, Singer RH (1995) Foci of trinucleotide repeat transcripts in nuclei of myotonic dystrophy cells and tissues. J Cell Biol 128: 995-1002
50. Timchenko NA, Cai ZJ, Welm AL, Reddy S, Ashizawa T, Timchenko LT (2001) RNA CUG repeats sequester CUGBP1 and alter protein levels and activity of CUGBP1. J Biol Chem 276: 7820-7826
51. Timchenko NA, Welm AL, Lu X, Timchenko LT (1999) CUG repeat binding protein (CUGBP1) interacts with the 5′ region of C/EBPbeta mRNA and regulates translation of C/EBPbeta isoforms. Nucleic Acids Res 27: 4517-4525
52. Wagner EJ, Garcia-Blanco MA (2002) RNAi-mediated PTB depletion leads to enhanced exon definition. Mol Cell 10: 943-949
53. Xu R, Teng J, Cooper TA (1993) The cardiac troponin T alternative exon contains a novel purine-rich positive splicing element. Mol Cell Biol 13: 3660-3674
54. Zhang L, Liu W, Grabowski PJ (1999) Coordinate repression of a trio of neuron-specific splicing events by the splicing regulator PTB. RNA 5: 117-130